Infective juveniles of entomopathogenic nematodes (Steinernema and Heterorhabditis) secrete ascarosides and respond to interspecific dispersal signals

Abstract

Ascarosides are a modular series of signalling molecules that are widely conserved in nematodes where they function as pheromones with both behavioural and developmental effects. Here we show that the developmentally arrested infective juvenile (IJ) stage of entomopathogenic nematodes (EPN) secrete ascarosides into the surrounding medium. The exometabolome of Steinernema carpocapsae and Heterorhabditis megidis was examined at 0, 1, 7 and 21 days of storage. The concentration of several ascarosides (ascr#11, ascr#9, ascr#12, ascr#1 and ascr#14 for both species, plus ascr#10 for H. megidis) showed a progressive increase over this period, while the concentration of longer chain ascarosides increased up to day 7, with an apparent decline thereafter. Ascr #9 was the main ascaroside produced by both species. Similar ascarosides were found over a 7-day period for Steinernema longicaudum and S. feltiae. Ascaroside blends have previously been shown to promote nematode dispersal. S. carpocapsae and H. megidis IJs were stored for up to 12 weeks and assayed at intervals. IJs where exometabolome was allowed to accumulate showed higher dispersal rates than those where water was changed frequently, indicating that IJ exometabolome maintained high dispersal. Infectivity was not affected. IJ exometabolome accumulated over 7 days promoted dispersal of freshly harvested IJs, both of their own and other EPN species. Similarly, extracts of nematode-infected cadavers promoted dispersal of con-and heterospecific IJs. Thus, IJs are encouraged to disperse from a source cadaver or from other crowded conditions by public information cues, a finding that may have application in enhancing biocontrol. However, the complexity of the ascaroside blend produced by IJs suggests that it may have ecological functions other than dispersal.

Conspecific and heterospecific pheromones stimulate dispersal of entomopathogenic nematodes during quiescence

“…Consistent with the literature, Hartley et al 39 showed that as the ascaroside content increases during storage and overall nematode dispersal was reduced from 1 to 3 weeks. When the IJs are exposed to one week-storage medium associated with high dispersal, it stimulates the IJ dispersal as expected 39 . However, the 3-week storage medium with lower dispersal activity has a different ascaroside composition.…”

“…In this study, S. carpocapsae IJs responded to pheromone extracts from consumed insect host cadavers of 8 different species of Steinernema and Heterorhabditis regardless of their foraging strategies. The literature and our current findings suggest that the pheromone mixtures have not diverged to the point where they are species specific 22,39,48 . However, the precise pheromone mix for each species remains to be discovered.…”

“…Ascarosides play a key role in EPN development and behaviors 22,29,[37][38][39][40][41] including preventing the recovery of IJs (analogous to the dauer stage in C. elegans), emergence from host cadavers after food depletion, and dispersal behavior after IJs emerge from the host 22,29 . While their significance is known, the specific compounds produced within an EPN system and their effects on behavior vary.…”

Photorhabdus: a tale of contrasting interactions

“…Therefore, the accumulation of the ascaroside signal effectively functions to counteract the IJ recovery activity of the bacteria-derived IPS molecule, thus allowing the nematode to halt reproduction in a nematode population-dependent manner. Indeed, it appears that, similar to what has been reported in C. elegans, Heterorhabditis nematodes produce a range of ascaroside-like molecules that can regulate both nematode development and behaviour [124][125][126]. However, it remains to be seen if Photorhabdus makes any contribution to the production and/or modification of these, or any other, nematode-derived signals.…”

Nematodes Follow a Leader

“…Recent research has shown a commonality in the production of and sensitivity to ascaroside pheromones among free-living, plantparasitic, and insect-parasitic nematode species (Choe et al, 2012). Given that these small signaling molecules coordinate development, can have multi-trophic effects (Noguez et al, 2012;Hsueh et al, 2013;Zhao et al, 2016), and affect social behaviors (Hartley et al, 2019;Kaplan et al, 2020;Meng et al, 2020), it follows that they may be involved in trail following, particularly for species where individuals would face challenges to their reproductive success without signals to attract potential mates. However, the implication of ascarosides here is speculative and needs careful analysis of chemicals involved.…”